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Salicylic acid biosynthesis is enhanced and contributes to increased biotrophic pathogen resistance in Arabidopsis hybrids.

Yang L, Li B, Zheng XY, Li J, Yang M, Dong X, He G, An C, Deng XW - Nat Commun (2015)

Bottom Line: Heterosis, the phenotypic superiority of a hybrid over its parents, has been demonstrated for many traits in Arabidopsis thaliana, but its effect on defence remains largely unexplored.Here, we show that hybrids between some A. thaliana accessions show increased resistance to the biotrophic bacterial pathogen Pseudomonas syringae pv. tomato (Pst) DC3000.Comparisons of transcriptomes between these hybrids and their parents after inoculation reveal that several key salicylic acid (SA) biosynthesis genes are significantly upregulated in hybrids.

View Article: PubMed Central - PubMed

Affiliation: 1] Peking-Yale Joint Center for Plant Molecular Genetics and Agro-Biotechnology, State Key Laboratory of Protein and Plant Gene Research, The Peking-Tsinghua Center for Life Sciences, School of Advanced Agricultural Sciences and School of Life Sciences, Peking University, Beijing 100871, China [2] Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, Connecticut 06520, USA.

ABSTRACT
Heterosis, the phenotypic superiority of a hybrid over its parents, has been demonstrated for many traits in Arabidopsis thaliana, but its effect on defence remains largely unexplored. Here, we show that hybrids between some A. thaliana accessions show increased resistance to the biotrophic bacterial pathogen Pseudomonas syringae pv. tomato (Pst) DC3000. Comparisons of transcriptomes between these hybrids and their parents after inoculation reveal that several key salicylic acid (SA) biosynthesis genes are significantly upregulated in hybrids. Moreover, SA levels are higher in hybrids than in either parent. Increased resistance to Pst DC3000 is significantly compromised in hybrids of pad4 mutants in which the SA biosynthesis pathway is blocked. Finally, increased histone H3 acetylation of key SA biosynthesis genes correlates with their upregulation in infected hybrids. Our data demonstrate that enhanced activation of SA biosynthesis in A. thaliana hybrids may contribute to their increased resistance to a biotrophic bacterial pathogen.

No MeSH data available.


Related in: MedlinePlus

Increased H3 acetylation correlates with altered expression of PAD4 and EDS1 in F1 hybrids.(a,b) qPCR analyses of PAD4 and EDS1 expression in F1 hybrids and parents of Col-0 × Sei-0 every 8 h post infiltration (hpi) up to 48 hpi with Pseudomonas syringae pv. tomato (Pst) DC3000 at 1 × 105 c.f.u. ml−1 or MgCl2. Fsc and Fcs, reciprocal F1 hybrids, where maternal line is Sei-0 and Col-0, respectively. Data are standardized for abundance of Actin transcript. (c,e) Regions of PAD4 and EDS1 used for ChIP–qPCR assays. (d,f) ChIP–qPCR analyses of promoter fragments (region 1) and exon fragments (region 2) of PAD4 and EDS1 in F1 hybrids and their parents using anti- H3Ac antibody at 1 dpi with Pst DC3000 or MgCl2, and ChIP–qPCR analyses of region 1 of PAD4 and EDS1 in F1 hybrids and their parents using anti-H3K27me3 antibody at 1 dpi with Pst DC3000. Error bars indicate s.d.. **P<0.01 between infiltrated with Pst DC3000 and MgCl2 of respective samples (Student's t-test). ChIP values were normalized to their respective DNA inputs. Data are shown as mean±s.d. The results are a representative of three biological repetitions. Error bars indicate s.d.. Data are shown as mean±s.d. (n=3, n means biological replication).
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f5: Increased H3 acetylation correlates with altered expression of PAD4 and EDS1 in F1 hybrids.(a,b) qPCR analyses of PAD4 and EDS1 expression in F1 hybrids and parents of Col-0 × Sei-0 every 8 h post infiltration (hpi) up to 48 hpi with Pseudomonas syringae pv. tomato (Pst) DC3000 at 1 × 105 c.f.u. ml−1 or MgCl2. Fsc and Fcs, reciprocal F1 hybrids, where maternal line is Sei-0 and Col-0, respectively. Data are standardized for abundance of Actin transcript. (c,e) Regions of PAD4 and EDS1 used for ChIP–qPCR assays. (d,f) ChIP–qPCR analyses of promoter fragments (region 1) and exon fragments (region 2) of PAD4 and EDS1 in F1 hybrids and their parents using anti- H3Ac antibody at 1 dpi with Pst DC3000 or MgCl2, and ChIP–qPCR analyses of region 1 of PAD4 and EDS1 in F1 hybrids and their parents using anti-H3K27me3 antibody at 1 dpi with Pst DC3000. Error bars indicate s.d.. **P<0.01 between infiltrated with Pst DC3000 and MgCl2 of respective samples (Student's t-test). ChIP values were normalized to their respective DNA inputs. Data are shown as mean±s.d. The results are a representative of three biological repetitions. Error bars indicate s.d.. Data are shown as mean±s.d. (n=3, n means biological replication).

Mentions: SA is a well-known hormone important for plant defence2829. That genes involved in the SA pathway changed significantly in hybrids relative to their parents suggests that enhanced activation of the SA pathway may be related to the increased resistance to Pst DC3000 in A. thaliana hybrids. To test this hypothesis, we extended our expression analysis by performing detailed time–course experiments. Leaf samples of hybrids and parents were collected every 8 h after infiltration up to 48 h and subjected to real-time quantitative reverse transcription PCR (qRT–PCR). As shown in Figs 3 and 5 and Supplementary Fig. 6, expression of PR1, PAD4, EDS1, SARD1 and CBP60g was significantly upregulated in the F1 hybrids of Col-0 × Sei-0 compared with their parents, and expression of these genes peaked in the hybrids 8 h earlier than in their parents. No expression changes were observed for these genes in the F1 hybrids of Col-0 × Aa-0 (Fig. 3b; Supplementary Fig. 7), which is consistent with the lack of evident heterosis for Pst DC3000 defence in these hybrids (Fig. 1). These results imply that the upregulation of key genes in the SA biosynthesis pathway in F1 hybrids may play a role in the increased resistance of hybrids to biotrophic bacterial pathogen.


Salicylic acid biosynthesis is enhanced and contributes to increased biotrophic pathogen resistance in Arabidopsis hybrids.

Yang L, Li B, Zheng XY, Li J, Yang M, Dong X, He G, An C, Deng XW - Nat Commun (2015)

Increased H3 acetylation correlates with altered expression of PAD4 and EDS1 in F1 hybrids.(a,b) qPCR analyses of PAD4 and EDS1 expression in F1 hybrids and parents of Col-0 × Sei-0 every 8 h post infiltration (hpi) up to 48 hpi with Pseudomonas syringae pv. tomato (Pst) DC3000 at 1 × 105 c.f.u. ml−1 or MgCl2. Fsc and Fcs, reciprocal F1 hybrids, where maternal line is Sei-0 and Col-0, respectively. Data are standardized for abundance of Actin transcript. (c,e) Regions of PAD4 and EDS1 used for ChIP–qPCR assays. (d,f) ChIP–qPCR analyses of promoter fragments (region 1) and exon fragments (region 2) of PAD4 and EDS1 in F1 hybrids and their parents using anti- H3Ac antibody at 1 dpi with Pst DC3000 or MgCl2, and ChIP–qPCR analyses of region 1 of PAD4 and EDS1 in F1 hybrids and their parents using anti-H3K27me3 antibody at 1 dpi with Pst DC3000. Error bars indicate s.d.. **P<0.01 between infiltrated with Pst DC3000 and MgCl2 of respective samples (Student's t-test). ChIP values were normalized to their respective DNA inputs. Data are shown as mean±s.d. The results are a representative of three biological repetitions. Error bars indicate s.d.. Data are shown as mean±s.d. (n=3, n means biological replication).
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f5: Increased H3 acetylation correlates with altered expression of PAD4 and EDS1 in F1 hybrids.(a,b) qPCR analyses of PAD4 and EDS1 expression in F1 hybrids and parents of Col-0 × Sei-0 every 8 h post infiltration (hpi) up to 48 hpi with Pseudomonas syringae pv. tomato (Pst) DC3000 at 1 × 105 c.f.u. ml−1 or MgCl2. Fsc and Fcs, reciprocal F1 hybrids, where maternal line is Sei-0 and Col-0, respectively. Data are standardized for abundance of Actin transcript. (c,e) Regions of PAD4 and EDS1 used for ChIP–qPCR assays. (d,f) ChIP–qPCR analyses of promoter fragments (region 1) and exon fragments (region 2) of PAD4 and EDS1 in F1 hybrids and their parents using anti- H3Ac antibody at 1 dpi with Pst DC3000 or MgCl2, and ChIP–qPCR analyses of region 1 of PAD4 and EDS1 in F1 hybrids and their parents using anti-H3K27me3 antibody at 1 dpi with Pst DC3000. Error bars indicate s.d.. **P<0.01 between infiltrated with Pst DC3000 and MgCl2 of respective samples (Student's t-test). ChIP values were normalized to their respective DNA inputs. Data are shown as mean±s.d. The results are a representative of three biological repetitions. Error bars indicate s.d.. Data are shown as mean±s.d. (n=3, n means biological replication).
Mentions: SA is a well-known hormone important for plant defence2829. That genes involved in the SA pathway changed significantly in hybrids relative to their parents suggests that enhanced activation of the SA pathway may be related to the increased resistance to Pst DC3000 in A. thaliana hybrids. To test this hypothesis, we extended our expression analysis by performing detailed time–course experiments. Leaf samples of hybrids and parents were collected every 8 h after infiltration up to 48 h and subjected to real-time quantitative reverse transcription PCR (qRT–PCR). As shown in Figs 3 and 5 and Supplementary Fig. 6, expression of PR1, PAD4, EDS1, SARD1 and CBP60g was significantly upregulated in the F1 hybrids of Col-0 × Sei-0 compared with their parents, and expression of these genes peaked in the hybrids 8 h earlier than in their parents. No expression changes were observed for these genes in the F1 hybrids of Col-0 × Aa-0 (Fig. 3b; Supplementary Fig. 7), which is consistent with the lack of evident heterosis for Pst DC3000 defence in these hybrids (Fig. 1). These results imply that the upregulation of key genes in the SA biosynthesis pathway in F1 hybrids may play a role in the increased resistance of hybrids to biotrophic bacterial pathogen.

Bottom Line: Heterosis, the phenotypic superiority of a hybrid over its parents, has been demonstrated for many traits in Arabidopsis thaliana, but its effect on defence remains largely unexplored.Here, we show that hybrids between some A. thaliana accessions show increased resistance to the biotrophic bacterial pathogen Pseudomonas syringae pv. tomato (Pst) DC3000.Comparisons of transcriptomes between these hybrids and their parents after inoculation reveal that several key salicylic acid (SA) biosynthesis genes are significantly upregulated in hybrids.

View Article: PubMed Central - PubMed

Affiliation: 1] Peking-Yale Joint Center for Plant Molecular Genetics and Agro-Biotechnology, State Key Laboratory of Protein and Plant Gene Research, The Peking-Tsinghua Center for Life Sciences, School of Advanced Agricultural Sciences and School of Life Sciences, Peking University, Beijing 100871, China [2] Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, Connecticut 06520, USA.

ABSTRACT
Heterosis, the phenotypic superiority of a hybrid over its parents, has been demonstrated for many traits in Arabidopsis thaliana, but its effect on defence remains largely unexplored. Here, we show that hybrids between some A. thaliana accessions show increased resistance to the biotrophic bacterial pathogen Pseudomonas syringae pv. tomato (Pst) DC3000. Comparisons of transcriptomes between these hybrids and their parents after inoculation reveal that several key salicylic acid (SA) biosynthesis genes are significantly upregulated in hybrids. Moreover, SA levels are higher in hybrids than in either parent. Increased resistance to Pst DC3000 is significantly compromised in hybrids of pad4 mutants in which the SA biosynthesis pathway is blocked. Finally, increased histone H3 acetylation of key SA biosynthesis genes correlates with their upregulation in infected hybrids. Our data demonstrate that enhanced activation of SA biosynthesis in A. thaliana hybrids may contribute to their increased resistance to a biotrophic bacterial pathogen.

No MeSH data available.


Related in: MedlinePlus